Spine and lower body symmetry during treadmill walking in healthy individuals—In-vivo 3-dimensional kinematic analysis

Although it is relevant to understand spine and lower body motions in healthy individuals for a variety of applications, such as clinical diagnosis, implant design, and the analysis of treatment outcomes, proper assessment and characterization of normative gait symmetry in healthy individuals remains unclear. The purpose of this study was to investigate the in vivo 3-dimensional (3D) spine and lower body gait symmetry kinematics during treadmill walking in healthy individuals. Sixty healthy young adults (30 males and 30 females) were evaluated during normal and fast treadmill walking using a motion capture system approach. Statistical parametric mapping and the normalized symmetry index approaches were used to determine spine, pelvis, and lower body asymmetries during treadmill walking. The spine and pelvis angular motions associated with the left and right lower limb motions, as well as the left and right lower extremity joint angles were compared for normal and fast treadmill walking. The lower lumbar left-right rotation (5.74±0.04°) and hip internal rotation (5.33±0.18°) presented the largest degrees of asymmetry during normal treadmill. Upper lumbar left-right lateral flexion (1.48±0.14°) and knee flexion (2.98±0.13°) indicated the largest asymmetries and during fast treadmill walking. Few asymmetry patterns were similar between normal and fast treadmill walking, whereas others appeared either only during normal or fast treadmill walking in this cohort of participants. These findings could provide insights into better understanding gait asymmetry in healthy individuals, and use them as reference indicators in diagnosing and evaluating abnormal gait function.


Introduction
The spine is the central supporting structure of the torso allowing for flexibility and shock absorption, as well as routing and protecting the spinal cord. The spine has been modeled as

Procedures and data collection
A power analysis based on our study results indicates that a sample size of 60 participants with an alpha = 0.05, and a sample ratio = 1, produces a power = 0.82. Upon arrival of the participants at the Ergonomics Laboratory of Universidad San Francisco de Quito, anthropometric data were collected. All participants first executed normal and fast level overground walking over a distance of 5 m for 4 times in separate trials. Participants were instructed to sustain a usual regular pace during normal overground walking, and accelerate their usual regular pace (as if they were in a hurry) during fast overground walking. The walking speeds of both conditions were recorded and used to set up the treadmill speeds. Participants were instructed to walk on a treadmill at normal and fast speeds under a 10-camera motion capture system (Vicon MX, Oxford, UK) surveillance sampling motion data at 100 Hz. A marker model of fifty-three reflective spherical markers (; 10 mm), based on previous studies [7,12,25], was used to obtained spine and lower body kinematics (Fig 1). The standard Vicon calibration procedures were applied to determine the 3D coordinates of the reflective spherical markers. Prior to data collection, each participant practiced for 5-minute on the treadmill. Each participant performed three trials that included at least ten complete gait cycles at normal and fast walking speeds. Thus, in total, each test condition had at least 30 complete gait cycles, and those were selected for analyses. The spine was defined as a kinematic chain of four segments, consisting of upper thorax (T1, T6, and two midpoint markers), lower thorax (T6, L1, and two midpoint markers), upper lumbar (L1, L3, and two midpoint markers), and the lower lumbar (L3, L5, and two midpoint markers) segments [7] (Fig 2). Local z axes were determined on spine segments between T1 and T6, T6 and L1, L1 and L3, and L3 and L5 for the upper thorax, lower thorax, upper lumbar, and lower lumbar segments, respectively. The local x axis, pointing anteriorly, of each spine segment was calculated by the cross product between the local z axis and the vector defined by the two midpoint markers (Fig 2). 3D angles of the upper thorax (between lower thorax and upper thorax), lower thorax (between upper lumbar and lower thorax), upper lumbar (between lower lumbar and upper lumbar), and lower lumbar (between pelvis and lower lumbar) were calculated (Fig 2). The cross product of opposite anterior superior iliac spine (ASIS) and posterior superior iliac spine (PSIS) left and right markers defined the local pelvis z axis, pointing upwards. The y axis, pointing laterally, was defined between left and right ASIS (Fig 2). Pelvis rotations were calculated relative to the global Vicon coordinate system (Fig 2). The long axes of the femur, tibia, and foot determined local z axes of each segment, respectively. Lateral and medial markers on the knee, ankle, and foot determined the local y axes, pointing laterally, of the femur, tibia, and foot, respectively [12,34]. Those axes were projected on thigh, tibia, and foot clusters and determined the 3D joint angles of the hip (between pelvis and femur), knee (between femur and tibia), and ankle (between foot and tibia) (Fig 2). Segment and joint angles were calculated using a Cardan angle sequence [35] (Fig 2). Data were exported and processed in MATLAB (MathWorks, Inc., Natick, MA) using a custom program.
The spine and pelvis 3D angular motions associated with the left and right lower limb movements, as well as the left and right lower extremity angular movements were compared for treadmill walking. Segment and joint angles for a standing relaxed pose were utilized as the zero neutral reference (Fig 2). The angular data was split into individual strides, and a time normalized waveform (0-100%) of the average gait cycle was generated with 1% sample steps [12,15,16], with 0% corresponding to heel contact of the concerned leg. Strides were defined to start with the initial contact and end with the following initial contact of one foot [23]. The 3D angles of the upper thorax, lower thorax, upper lumbar, lower lumbar and pelvis segments, as well as the hip, knee, and ankle joints were calculated to evaluate spine, pelvis and lower body kinematic gait symmetry.
Symmetry was calculated throughout the gait cycle for spine, pelvis, and lower body motions. Statistical parametric mapping and the normalized symmetry index, presented by Gouwanda et al. [21], were calculated for assessing gait symmetry of the spine and pelvis angular motions, as well as lower body joint angles. The normalized symmetry index (SI norm ) was calculated based on Eq 1 [19][20][21]23].

Statistical analysis
The software MATLAB (MathWorks, Inc., Natick, MA) was used to performed SPM [12,[36][37][38] analyses using scalar fields to determine significant differences between the spine and pelvis angular motions associated with the left lower limb motions, and spine and pelvis angular motions associated with the right lower limb motions, as well as between the left and right hip, knee, and ankles joint angles throughout the gait cycle. A Student's t-test was used to compare maximum SI norm differences between normal and fast treadmill walking. Likewise, A Student's t-test compared walking speeds for each condition. A significance level of α = 0.05 was used for the analysis. Local z axes were determined between T1 and T6, T6 and L1, L1 and L3, and L3 and L5 for upper thorax, lower thorax, upper lumbar, and lower lumbar segments, respectively. Cross product of the z axis and the vector defined by the two midpoint markers determined the x axis of each spine segment. Joint angles defined for the upper thorax, lower thorax, upper lumbar, and lower lumbar. The left and right anterior superior iliac spine (ASIS) and posterior superior iliac spine (PSIS) markers defined the local pelvis axes, with the y axis defined between left and right ASIS, and the x axis pointing anteriorly. Anatomical hip, knee, ankle joint axes were projected on thigh, tibia, and foot clusters, respectively, with the local z axis along the long axis of the femur, tibia, and foot, and the local y axis pointing laterally. Asymmetric spine motion during normal treadmill walking SPM analysis indicated that the upper and lower thorax segments presented symmetrical angular motions during normal treadmill walking, as the scalar field SPM curve did not exceed the threshold t � for α = 0.05 (Fig 3). SI norm values for upper and lower thorax flexion-extension varied between ±35% whereas the left-right lateral flexion and left-right rotation varied between ±15% (Fig 3). SPM indicated that upper and lower lumbar angular motions were asymmetrical. The upper lumbar indicated an asymmetrical flexion-extension at 45-52% and 93-99% of the gait cycle, with SI norm values varying between ±35% (Fig 3). The upper lumbar left-right lateral flexion was asymmetrical throughout the normal treadmill walking cycle, with SI norm values changing between ±15% (Fig 3). No asymmetrical motion was detected for the upper lumbar left-right rotation, and the SI norm values varied between ±12% (Fig 3). The lower lumbar flexion-extension was asymmetrical at 2-3%, 4-16%, and 56-66% of the gait cycle, with the SI norm values varying between ±28% (Fig 3). The lower lumbar left-right lateral flexion was asymmetrical at 1-8%, 14-45%, 60-98%, and 99-100% of the gait cycle, with the SI norm values varying between ±14% (Fig 3). The lower lumbar left-right rotation was asymmetrical during the complete gait cycle, with the SI norm values changing between ±13% (Fig 3).

Asymmetric spine motions during fast treadmill walking
SPM analysis showed that the upper and lower thorax segments presented symmetrical angular motions during fast treadmill walking (Fig 4). SI norm values for upper and lower thorax flexion-extension varied between ±36% whereas the left-right lateral flexion and left-right rotation varied between ±17% (Fig 4). SPM indicated that upper and lower lumbar angular motions were asymmetrical. The upper lumbar indicated a symmetricalflexion-extension, with SI norm values varying between ±25% (Fig 4). The upper lumbar left-right lateral flexion was asymmetrical throughout the fast treadmill walking cycle, with SI norm values changing between ±14% (Fig 4). The upper lumbar presented an asymmetrical left-right rotation at 13-20% and 60-73% of the gait cycle, with the SI norm values varying between ±12% (Fig 4). The lower lumbar flexion-extension was asymmetrical at 9-19% and 58-68% of the gait cycle, with the SI norm values varying between ±29% (Fig 4). The lower lumbar left-right lateral flexion was symmetrical, and the SI norm values varied between ±14% (Fig 4). The lower lumbar left-right rotation was symmetrical, and the SI norm values changed between ±14% (Fig 4). Descriptive statistics of the average degree of asymmetry, describing the mean difference between left and right-side movements when the scalar field SPM detected significant differences, and the maximum magnitude of the SI norm when the scalar field SPM detected significant differences, in spine segments during normal and fast treadmill walking are presented in Table 1.

Asymmetric lower body motions during normal treadmill walking
Pelvis posterior-anterior tilt was asymmetrical at 30-40%, 48-49%, and 76-93% of the gait cycle, with the SI norm values changing between ±25% (Fig 5). Pelvis left-rightobliquity was asymmetrical throughout the normal treadmill walking cycle, with SI norm values changing between ±12% (Fig 5). No asymmetries were detected for pelvis left-right rotations, and the SI norm values varied between ±11% (Fig 5). Significant flexion-extension asymmetries were detected between left and right hips at 15-55% of the normal treadmill walking cycle, with SI norm values varying between ±12% (Fig 5). Adduction-abduction of left and right hips were symmetrical, and the SI norm values varied between ±18% (Fig 5). Hip internal-external rotation was asymmetrical at 4-10% and 68-78% of the gait cycle, with SI norm values varying between ±23% (Fig 5). Right knees were more flexed than the left ones at 5-39% and 82-97% of the gait cycle, with SI norm values varying between ±8% (Fig 5). No asymmetries were detected for knee adduction-abduction, and the SI norm values varied between ±22% (Fig 5). Left knees had less internal rotation than the right knees at 4-10%, 16-17%, 22-42%, 83-87%, and 96-97% of the gait cycle, with SI norm values varying between ±20% (Fig 5). Neither ankle dorsi-plantar flexion nor internal-external rotation were asymmetrical during normal treadmill walking, and the SI norm values varied between ±10% and ±29%, respectively (Fig 5). Yet, the right ankles had more eversion than the left ones at 0-19% and 71-100% of the gait cycle, with SI norm values varying between ±16% (Fig 5). The standard deviation of the left side was higher than the right side for hip, knee, and ankle motions (Fig 5).

Asymmetric lower body motions during fast treadmill walking
Pelvis posterior-anterior tilt was asymmetrical at 0-13%, 36-63%, and 84-100% of the gait cycle, with the SI norm values changing between ±29% (Fig 6). Pelvis left-right obliquity was asymmetrical at 4-22% and 53-66% of the gait cycle, with the SI norm values changing between ±11% (Fig 6). No asymmetries were detected for pelvis left-right rotations, and the SI norm values varied between ±11% (Fig 6). Significant flexion-extension asymmetries were detected between left and right hips at 19-53% of the fast treadmill walking cycle, with SI norm values varying between ±10% (Fig 6). Adduction-abduction of left and right hips were symmetrical, and the SI norm values varied between ±19% (Fig 6). Hip internal-external rotation was symmetrical, and SI norm values varied between ±22% (Fig 6). Right knees were more flexed than the left ones at 0-42% and 81-100% of the gait cycle, with SI norm values varying between ±9% (Fig 6). No asymmetries were detected for knee adduction-abduction, and the SI norm values varied between ±21% (Fig 6). Left knees had less internal rotation than the right knees at 0-20%, 25-40%, and 95-100% of the gait cycle, with SI norm values varying between ±21% ( Fig  6). Ankle dorsi-plantar flexion was asymmetrical at 12-13%,35-37%, 45-48% and 79-94% of the gait cycle, with SI norm values varying between ±12% (Fig 6). Ankle eversion-inversion was symmetrical, and the SI norm values varied between ±15% (Fig 6). Ankle internal-external rotation was asymmetrical at 92-98% of the gait cycle, with the SI norm values changing between ±22% (Fig 6). The standard deviation of the left side was higher than the right side for hip, knee, and ankle motions (Fig 6).

Fig 5. Average and standard deviation of pelvis posterior-anterior (P/A) tilt, left-right(L/R) obliquity, and (L/R) rotation, hip and knee flexion-extension (F/E), adduction-abduction (Ad/Ab), and internal-external (Int/Ext) rotation, and ankle dorsi-plantar flexion (DF/PF), eversion-inversion (Eve/Inv), and internal-external (Int/Ext) rotation for left and right sides during one gait cycle of normal treadmill walking (TWN) in sixty healthy participants.
Green bars on the horizontal axis and the scalar field SPM results with threshold t � t depict where, in % cycle, left side angles were greater or lesser than right side angles. Descriptive statistics of the average degree of asymmetry, describing the mean difference between left and right-side movements when the scalar field SPM detected significant differences, and the maximum magnitude of the SI norm when the scalar field SPM detected significant differences, in the pelvis segment and lower body joints during normal and fast treadmill walking are presented in Table 2.
Descriptive statistics of the SI norm and its comparison between normal and fast treadmill walking is presented in Table 3. Overall, greater asymmetries were found during fast treadmill walking than normal treadmill walking.

Discussion
The purpose of the present study was to examine 3D spine, pelvis, and lower body symmetry kinematics in young healthy individuals throughout the gait cycle during normal and fast treadmill walking. Our analysis revealed significant asymmetries in upper lumbar, lower lumbar, and pelvis segments, as well as in hip, knee, and ankle joints during normal and fast treadmill walking. Degrees of asymmetry and the associated maximum magnitude of SI norm of 5.74 ±0.04˚and 14%, as well as 5.33±0.18˚and 21%, for the lower lumbar left-right rotation and hip internal rotation, respectively, were the largest asymmetries detected during normal treadmill walking. Upper lumbar left-right lateral flexion and knee flexion-extension with degrees of asymmetry and the associated the maximum magnitude of SI norm of 1.48±0.14˚and 15.3%, as well as 2.98±0.13˚and 6.5%, respectively, were the largest asymmetries found during fast treadmill walking. The current analysis revealed that few asymmetry patterns were similar

Fig 6. Average and standard deviation of pelvis posterior-anterior (P/A) tilt, left-right (L/R) obliquity, and (L/R) rotation, hip and knee flexion-extension (F/E), adduction-abduction (Ad/Ab), and internal-external (Int/Ext) rotation, and ankle dorsi-plantar flexion (DF/PF), eversion-inversion (Eve/Inv), and internal-external (Int/Ext) rotation for left and right sides during one gait cycle of normal treadmill walking (TWN) in sixty healthy participants.
Green bars on the horizontal axis and the scalar field SPM results with threshold t � t depict where, in % cycle, left side angles were greater or lesser than right side angles. The normalized symmetry index (SI norm ) calculated during one gait cycle of TWN. Solid and dashed lines correspond to average left and right sides, as well as average SI norm , and shaded areas correspond to standard deviation. Black dotted vertical lines denote toe-off. between normal and fast treadmill walking, whereas others appeared either only during normal or fast treadmill walking. These results rejected the null hypothesis of no difference in spine, pelvis, and lower body motions between left and right sides during normal and fast treadmill walking in healthy individuals.

Segment
Treadmill It has been reported that the walking speed affects individuals' gait kinematics [39,40]; however, the influence of treadmill walking speed on gait symmetry kinematics in healthy individuals remains unclear. Overall, our findings suggest that young healthy adults may be more asymmetrical during fast treadmill walking than normal treadmill walking (see Table 3). In addition, our results revealed standard deviations of the left side higher than the right side for hip, knee, and ankle motions during normal and fast treadmill walking. A possible explanation for this difference may be related to laterality [41], as in our study, 52 out 60 participants reported to be right-dominant, with leg dominance being defined as the preferred leg for kicking a ball. Even though previous reports indicate that walking slowly is more challenging to the motor control of gait than usual and faster speed walks [42,43], differences of gait motor control between usual and faster speed walking are not clear. Therefore, the findings of this study reported as the degree of asymmetry and the normalized symmetry index may be useful indicators of the gait motor control at different walking speeds.
Previous studies have investigated spine and lower body gait kinematics [6,8,9,[24][25][26][27]. In addition, although several studies have investigated on gait symmetry [17][18][19][20][21][22][23]44] and presented valuable information, there is not generally accepted standard for characterization of gait symmetry [23]. Asymmetric gait patterns in healthy individuals may be expected as there exist natural functional differences between the lower extremities [12,41,42], such as the contribution of each limb in carrying out the tasks of propulsion and control during able-bodied walking [41]. The present study provides information not only on the degree of asymmetry, the mean angular difference between left and right sides, but also on the SI norm in healthy individuals during normal and fast treadmill walking. Such information will add to the knowledge provided by previous investigations to better understand spine, pelvis, and lower body motions in healthy individuals. Our findings on SI norm for lower body motions in the sagittal plane were comparable to the ones described in [23]. Moreover, this study adds information on the SI norm parameter by describing the spine and pelvis 3D angular motions. In addition, reference degree of asymmetry information in healthy individuals has been presented in this study to help in the biomechanical assessment pathological individuals. Although the use of this indicator may be confusing as it is not referenced to the joint range of motion, such indicator has been implemented to assess asymmetry in pathological individuals. For instance, the degrees of asymmetry reported in total hip [16,28,29] and knee [15] replacement patients are greater than the degrees of asymmetry observed in the present study. Consequently, degrees of asymmetry greater than the ones reported in this study may be an indicative of abnormal gait function. Several limitations need to be considered to interpret the present results. To begin with, the average age of the male and female participants in this study was~21 years old, 52 out of 60 participants reported to be right-dominant, and all participants reported a healthy lifestyle (exercised at least twice a week); hence, results may be limited to similar populations. Furthermore, few gait cycles (~30) were used in normal and fast treadmill walking conditions; hence, the long terms of gait asymmetry kinematics were not explored. Additionally, participants wore different types of shoes during the experiments; thus, the influence of distinct shoes was not investigated in this study. Moreover, the skin-marker-based tracking technique used in this study is vulnerable to soft tissue artifacts [45]; however, clusters of at least four markers were used in each segment to reduce the influence of soft tissue artifacts. In addition, no ground reaction force, or electromyography (EMG) data was used in this study and thus, neither body kinetics, nor muscle activation patterns, were included. Future studies should include joint kinetics, ground reaction forces, and EMG data to gain a better understanding of asymmetry patterns in gait biomechanics.

Conclusions
The present study revealed significant asymmetries in upper lumbar, lower lumbar, and pelvis segments, as well as in hip, knee, and ankle joints during normal and fast treadmill walking. Few asymmetry patterns were similar between normal and fast treadmill walking, whereas others appeared either only during normal or fast treadmill walking. Our findings suggest that young healthy adults may be more asymmetrical during fast treadmill walking than normal treadmill walking. The current study methodology allows for observation of asymmetries throughout the gait cycle and introduces reference values based on two symmetry indicators. These findings could provide insights into better understanding gait asymmetry in healthy individuals, and use them as reference indicators in diagnosing and evaluating abnormal gait function.